CB2-receptor stimulation attenuates TNF-α-induced human endothelial cell activation, transendothelial migration of monocytes, and monocyte-endothelial adhesion

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 293, Issue 4, 2007, Pages

  Rajesh, Mohanraj ^a   Mukhopadhyay, Partha ^a   Bátkai, Sándor ^a   Haskó, György ^b   Liaudet, Lucas ^c   Huffman, John W ^d   Csiszar, Anna ^e   Ungvari, Zoltan ^e   Mackie, Ken ^f   Chatterjee, Subroto ^g   Pacher, Pál ^a  

^a NATIONAL INSTITUTE ON ALCOHOL ABUSE AND ALCOHOLISM   (United States)

^b RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

^c LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

^d CLEMSON UNIVERSITY   (United States)

^e NEW YORK MEDICAL COLLEGE   (United States)

^f INDIANA UNIVERSITY   (United States)

^g JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Adhesion molecules; Endothelial activation; Inflammation; RhoA

Indexed keywords

1 DEOXY 3 (1,1 DIMETHYLBUTYL) DELTA8 TETRAHYDROCANNABINOL; 4 [4 (1,1 DIMETHYLHEPTYL) 2,6 DIMETHOXYPHENYL] 6,6 DIMETHYLBICYCLO[3.1.1]HEPT 2 EN 2 YLMETHANOL; 5 (4 CHLORO 3 METHYLPHENYL) 1 (4 METHYLBENZYL) N (1,3,3 TRIMETHYLBICYCLO[2.2.1]HEPTAN 2 YL) 3 PYRAZOLECARBOXAMIDE; 6 IODO 3 (4 METHOXYBENZOYL) 2 METHYL 1 (2 MORPHOLINOETHYL)INDOLE; CANNABINOID 1 RECEPTOR; CANNABINOID 2 RECEPTOR; ENDOTOXIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERCELLULAR ADHESION MOLECULE 1; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; RIMONABANT; TUMOR NECROSIS FACTOR ALPHA; VASCULAR CELL ADHESION MOLECULE 1; 1,1 DIMETHYLBUTYL 1 DEOXY DELTA(9) THC; 1,1-DIMETHYLBUTYL-1-DEOXY-DELTA(9)-THC; ANTIINFLAMMATORY AGENT; CANNABINOID; CCL2 PROTEIN, HUMAN; LIPOPOLYSACCHARIDE; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; UNCLASSIFIED DRUG;

ADOLESCENT; ANIMAL CELL; ANIMAL EXPERIMENT; ANTIINFLAMMATORY ACTIVITY; AORTA; ARTICLE; ATHEROSCLEROSIS; CELL ACTIVATION; CELL ADHESION; CELL MIGRATION; CORONARY ARTERY; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; INFLAMMATORY DISEASE; MALE; MONOCYTE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REAL TIME POLYMERASE CHAIN REACTION; RECEPTOR UPREGULATION; RESTENOSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; VASCULAR ENDOTHELIUM; WESTERN BLOTTING; ANIMAL; C57BL MOUSE; CELL CULTURE; CHEMICALLY INDUCED DISORDER; CORONARY BLOOD VESSEL; DISEASE MODEL; DOSE RESPONSE; DRUG EFFECT; DRUG POTENTIATION; GENETICS; INFLAMMATION; LEUKOCYTE ROLLING; METABOLISM;

ANIMALS; ANTI-INFLAMMATORY AGENTS; AORTA; CANNABINOIDS; CELLS, CULTURED; CHEMOKINE CCL2; CORONARY VESSELS; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; ENDOTHELIAL CELLS; HUMANS; INFLAMMATION; INTERCELLULAR ADHESION MOLECULE-1; LEUKOCYTE ROLLING; LIPOPOLYSACCHARIDES; MALE; MICE; MICE, INBRED C57BL; MONOCYTES; NF-KAPPA B; RECEPTOR, CANNABINOID, CB1; RECEPTOR, CANNABINOID, CB2; RHOA GTP-BINDING PROTEIN; RNA, MESSENGER; SIGNAL TRANSDUCTION; TUMOR NECROSIS FACTOR-ALPHA; VASCULAR CELL ADHESION MOLECULE-1;

EID: 35348946336     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00688.2007     Document Type: Article

References (52)

1. Batkai S, Osei-Hyiaman D, Pan H, El-Assal O, Rajesh M, Mukhopadhyay P, Hong F, Harvey-White J, Jafri A, Hasko G, Huffman JW, Gao B, Kunos G, Pacher P. Cannabinoid-2 receptor mediates protection against hepatic ischemia/reperfusion injury. FASEB J 21: 1788-1800, 2007.
2. Bhunia AK, Arai T, Bulkley G, Chatterjee S. Lactosylceramide mediates tumor necrosis factor-alpha-induced intercellular adhesion molecule-1 (ICAM-1) expression and the adhesion of neutrophil in human umbilical vein endothelial cells. J Biol Chem 273: 34349-34357, 1998.
3. Blazquez C, Casanova ML, Planas A, Del Pulgar TG, Villanueva C, Fernandez-Acenero MJ, Aragones J, Huffman JW, Jorcano JL, Guzman M. Inhibition of tumor angiogenesis by cannabinoids. FASEB J 17: 529-531, 2003.
4. Branen L, Hovgaard L, Nitulescu M, Bengtsson E, Nilsson J, Jovinge S. Inhibition of tumor necrosis factor-α reduces atherosclerosis in apolipoprotein E knockout mice. Arterioscler Thromb Vasc Biol 24: 2137-2142, 2004.
5. Chatterjee S, Wei H. Roles of glycosphingolipids in cell signaling: adhesion, migration, and proliferation. Methods Enzymol 363: 300-312, 2003.
6. Csiszar A, Ahmad M, Smith KE, Labinskyy N, Gao Q, Kaley G, Edwards JG, Wolin MS, Ungvari Z. Bone morphogenetic protein-2 induces proinflammatory endothelial phenotype. Am J Pathol 168: 629-638, 2006.
7. Di Filippo C, Rossi F, Rossi S, D'Amico M. Cannabinoid CB2 receptor activation reduces mouse myocardial ischemia-reperfusion injury: involvement of cytokine/chemokines and PMN. J Leukoc Biol 75: 453-459, 2004.
8. Ghosh S, Preet A, Groopman JE, Ganju RK. Cannabinoid receptor CB2 modulates the CXCL12/CXCR4-mediated chemotaxis of T lymphocytes. Mol Immunol 43: 2169-2179, 2006.
9. Golech SA, McCarron RM, Chen Y, Bembry J, Lenz F, Mechoulam R, Shohami E, Spatz M. Human brain endothelium: coexpression and function of vanilloid and endocannabinoid receptors. Brain Res 132: 87-92, 2004.
10. Hansson GK, Libby P. The immune response in atherosclerosis: a double-edged sword. Nat Rev 6: 508-519, 2006.
11. 2, a peripheral cannabinoid receptor. Proc Natl Acad Sci USA 96: 14228-14233, 1999.
12. Harrison D, Griendling KK, Landmesser U, Hornig B, Drexler H. Role of oxidative stress in atherosclerosis. Am J Cardiol 91: 7A-11A, 2003.
13. Huffman JW, Liddle J, Yu S, Aung MM, Abood ME, Wiley JL, Martin BR. 3-(1′,1′-Dimethylbutyl)-1-deoxy-δ8-THC and related compounds: synthesis of selective ligands for the CB2 receptor. Bioorg Med Chem 7: 2905-2914, 1999.
14. Ip JH, Fuster V, Badimon L, Badimon J, Taubman MB, Chesebro JH. Syndromes of accelerated atherosclerosis: role of vascular injury and smooth muscle cell proliferation. J Am Coll Cardiol 15: 1667-1687, 1990.
15. Jaeschke H. Cellular adhesion molecules: regulation and functional significance in the pathogenesis of liver diseases. Am J Physiol Gastrointest Liver Physiol 273: G602-G611, 1997.
16. Jaeschke H, Smith CW. Mechanisms of neutrophil-induced parenchymal cell injury. J Leukoc Biol 61: 647-653, 1997.
17. Javaid K, Rahman A, Anwar KN, Frey RS, Minshall RD, Malik AB. Tumor necrosis factor-α induces early-onset endothelial adhesivity by protein kinase Cζ-dependent activation of intercellular adhesion molecule-1. Circ Res 92: 1089-1097, 2003.
18. Jawien J, Gajda M, Mateuszuk L, Olszanecki R, Jakubowski A, Szlachcic A, Korabiowska M, Korbut R. Inhibition of nuclear factor-κB attenuates artherosclerosis in apoE/LDLR-double knockout mice. J Physiol Pharmacol 56: 483-489, 2005.
19. Klein TW. Cannabinoid-based drugs as anti-inflammatory therapeutics. Nat Rev 5: 400-411, 2005.
20. Li Y, Schwabe RF, DeVries-Seimon T, Yao PM, Gerbod-Giannone MC, Tall AR, Davis RJ, Flavell R, Brenner DA, Tabas I. Free cholesterol-loaded macrophages are an abundant source of tumor necrosis factor-α and interleukin-6: model of NF-κB- and MAP kinase-dependent inflammation in advanced atherosclerosis. J Biol Chem 280: 21763-21772, 2005.
21. Lockyer JM, Colladay JS, Alperin-Lea WL, Hammond T, Buda AJ. Inhibition of nuclear factor-κB-mediated adhesion molecule expression in human endothelial cells. Circ Res 82: 314-320, 1998.
22. Mackie K. Cannabinoid receptors as therapeutic targets. Annu Rev Pharmacol Toxicol 46: 101-122, 2006.
23. Maier W, Altwegg LA, Corti R, Gay S, Hersberger M, Maly FE, Sutsch G, Roffi M, Neidhart M, Eberli FR, Tanner FC, Gobbi S, von Eckardstein A, Luscher TF. Inflammatory markers at the site of ruptured plaque in acute myocardial infarction: locally increased interleukin-6 and serum amyloid A but decreased C-reactive protein. Circulation 111: 1355-1361, 2005.
24. Marui N, Offermann MK, Swerlick R, Kunsch C, Rosen CA, Ahmad M, Alexander RW, Medford RM. Vascular cell adhesion molecule-1 (VCAM-1) gene transcription and expression are regulated through an antioxidant-sensitive mechanism in human vascular endothelial cells. J Clin Invest 92: 1866-1874, 1993.
25. Mestre L, Correa F, Docagne F, Clemente D, Guaza C. The synthetic cannabinoid WIN 55,212-2 increases COX-2 expression and PGE2 release in murine brain-derived endothelial cells following Theiler's virus infection. Biochem Pharmacol 72: 869-880, 2006.
26. Mukhopadhyay P, Batkai S, Rajesh M, Czifra N, Harvey-White J, Hasko G, Zsengeller Z, Gerard NP, Liaudet L, Kunos G, Pacher P. Pharmacological inhibition of cannabinoid receptor-1 protects against doxorubicin-induced cardiotoxicity. J Am Coll Cardiol 50: 528-536, 2007.
27. Ohta H, Wada H, Niwa T, Kirii H, Iwamoto N, Fujii H, Saito K, Sekikawa K, Seishima M. Disruption of tumor necrosis factor-α gene diminishes the development of atherosclerosis in ApoE-deficient mice. Atherosclerosis 180: 11-17, 2005.
28. Osterud B, Bjorklid E. Role of monocytes in atherogenesis. Physiol Rev 83: 1069-1112, 2003.
29. Pacher P, Batkai S, Kunos G. The endocannabinoid system as an emerging target of pharmacotherapy. Pharmacol Rev 58: 389-462, 2006.
30. Pacher P, Beckman JS, Liaudet L. Nitric oxide and peroxynitrite in health and disease. Physiol Rev 87: 315-424, 2007.
31. Patel RP, Moellering D, Murphy-Ullrich J, Jo H, Beckman JS, Darley-Usmar VM. Cell signaling by reactive nitrogen and oxygen species in atherosclerosis. Free Radic Biol Med 28: 1780-1794, 2000.
32. Rajesh M, Pan H, Mukhopadhyay P, Batkai S, Osei-Hyiaman D, Hasko G, Liaudet L, Gao B, Pacher P. Cannabinoid-2 receptor agonist HU-308 protects against hepatic ischemia/reperfusion injury by attenuating oxidative stress, inflammatory response and apoptosis. J Leukoc Biol In press.
33. Seasholtz TM, Brown JH. RHO SIGNALING in vascular diseases. Mol Interv 4: 348-357, 2004.
34. Shmist YA, Goncharov I, Eichler M, Shneyvays V, Isaac A, Vogel Z, Shainberg A. δ-9-Tetrahydrocannabinol protects cardiac cells from hypoxia via CB2 receptor activation and nitric oxide production. Mol Cell Biochem 283: 75-83, 2006.
35. Skoog T, Dichtl W, Boquist S, Skoglund-Andersson C, Karpe F, Tang R, Bond MG, de Faire U, Nilsson J, Eriksson P, Hamsten A. Plasma tumour necrosis factor-α and early carotid atherosclerosis in healthy middle-aged men. Eur Heart J 23: 376-383, 2002.
36. Spiecker M, Darius H, Liao JK. A functional role of IκB-epsilon in endothelial cell activation. J Immunol 164: 3316-3322, 2000.
37. Stamatovic SM, Keep RF, Kunkel SL, Andjelkovic AV. Potential role of MCP-1 in endothelial cell tight junction "opening": signaling via Rho and Rho kinase. J Cell Sci 116: 4615-4628, 2003.
38. Steffens S, Veillard NR, Arnaud C, Pelli G, Burger F, Staub C, Karsak M, Zimmer A, Frossard JL, Mach F. Low dose oral cannabinoid therapy reduces progression of atherosclerosis in mice. Nature 434: 782-786, 2005.
39. Stoll LL, Denning GM, Weintraub NL. Endotoxin, TLR4 signaling and vascular inflammation: potential therapeutic targets in cardiovascular disease. Current Pharm Design 12: 4229-4245, 2006.
40. Stoll LL, Denning GM, Weintraub NL. Potential role of endotoxin as a proinflammatory mediator of atherosclerosis. Arterioscler Thromb Vasc Biol 24: 2227-2236, 2004.
41. Takahashi M, Masuyama J, Ikeda U, Kasahara T, Kitagawa S, Takahashi Y, Shimada K, Kano S. Induction of monocyte chemoattractant protein-1 synthesis in human monocytes during transendothelial migration in vitro. Circ Res 76: 750-757, 1995.
42. Takeda R, Suzuki E, Satonaka H, Oba S, Nishimatsu H, Omata M, Fujita T, Nagai R, Hirata Y. Blockade of endogenous cytokines mitigates neointimal formation in obese Zucker rats. Circulation 111: 1398-1406, 2005.
43. Tedgui A, Mallat Z. Cytokines in atherosclerosis: pathogenic and regulatory pathways. Physiol Rev 86: 515-581, 2006.
44. Tzoulaki I, Murray GD, Lee AJ, Rumley A, Lowe GD, Fowkes FG. C-reactive protein, interleukin-6, and soluble adhesion molecules as predictors of progressive peripheral atherosclerosis in the general population: Edinburgh Artery Study. Circulation 112: 976-983, 2005.
45. Van Sickle MD, Duncan M, Kingsley PJ, Mouihate A, Urbani P, Mackie K, Stella N, Makriyannis A, Piomelli D, Davison JS, Marnett LJ, Di Marzo V, Pittman QJ, Patel KD, Sharkey KA. Identification and functional characterization of brainstem cannabinoid CB2 receptors. Science 310: 329-332, 2005.
46. Walter L, Franklin A, Witting A, Wade C, Xie Y, Kunos G, Mackie K, Stella N. Nonpsychotropic cannabinoid receptors regulate microglial cell migration. J Neurosci 23: 1398-1405, 2003.
47. Weber C, Erl W, Pietsch A, Weber PC. Aspirin inhibits nuclear factor-κB mobilization and monocyte adhesion in stimulated human endothelial cells. Circulation 91: 1914-1917, 1995.
48. Wung BS, Ni CW, Wang DL. ICAM-1 induction by TNF-α and IL-6 is mediated by distinct pathways via Rac in endothelial cells. J Biomed Sci 12: 91-101, 2005.
49. Zhang M, Martin BR, Adler MW, Razdan RK, Jallo JI, Tuma RF. Cannabinoid CB(2) receptor activation decreases cerebral infarction in a mouse focal ischemia/reperfusion model. J Cereb Blood Flow Metab 27: 1387-1396, 2007.
50. Zhang WJ, Frei B. α-Lipoic acid inhibits TNF-α-induced NF-κB activation and adhesion molecule expression in human aortic endothelial cells. FASEB J 15: 2423-2432, 2001.
51. Zhang WJ, Wei H, Hagen T, Frei B. α-Lipoic acid attenuates LPS-induced inflammatory responses by activating the phosphoinositide 3-kinase/Akt signaling pathway. Proc Natl Acad Sci USA 104: 4077-4082, 2007.
52. 2+ signaling via CB2 receptor linked to phospholipase C in calf pulmonary endothelial cells. Br J Pharmacol 140: 1351-1362, 2003.